A postmeiotically bifurcated roadmap of honeybee spermatogenesis marked by phylogenetically restricted genes
Open Access
- 4 December 2023
- journal article
- research article
- Published by Public Library of Science (PLoS) in PLOS Genetics
- Vol. 19 (12) , e1011081
Abstract
Haploid males of hymenopteran species produce gametes through an abortive meiosis I followed by meiosis II that can either be symmetric or asymmetric in different species. Thus, one spermatocyte could give rise to two spermatids with either equal or unequal amounts of cytoplasm. It is currently unknown what molecular features accompany these postmeiotic sperm cells especially in species with asymmetric meiosis II such as bees. Here we present testis single-cell RNA sequencing datasets from the honeybee (Apis mellifera) drones of 3 and 14 days after emergence (3d and 14d). We show that, while 3d testes exhibit active, ongoing spermatogenesis, 14d testes only have late-stage spermatids. We identify a postmeiotic bifurcation in the transcriptional roadmap during spermatogenesis, with cells progressing toward the annotated spermatids (SPT) and small spermatids (sSPT), respectively. Despite an overall similarity in their transcriptomic profiles, sSPTs express the fewest genes and the least RNA content among all the sperm cell types. Intriguingly, sSPTs exhibit a relatively high expression level for Hymenoptera-restricted genes and a high mutation load, suggesting that the special meiosis II during spermatogenesis in the honeybee is accompanied by phylogenetically young gene activities.Keywords
Funding Information
- Key Technologies Research and Development Program (2018YFA0800102)
- Key Technologies Research and Development Program (2021YFC2700403)
- National Natural Science Foundation of China (31871249)
- National Natural Science Foundation of China (31871452)
- Key Technologies Research and Development Program (2022YFD1600205)
- Agriculture Research System of China (NYCYTX-44-KXJ5)
- Agricultural Science and Technology Innovation Program Chinese Academy of Agricultural Sciences (CAAS-ASTIP-2023-IAR)
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